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Causes, Effects and Molecular Mechanisms of Testicular Heat Stress

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Causes, Effects and Molecular Mechanisms of Testicular Heat Stress ARTICLE IN PRESS Reproductive BioMedicine Online (2014) ■■, ■■–■■ www.sciencedirect.com www.rbmonline.com REVIEW Causes, effects and molecular mechanisms of testicular heat stress Damayanthi Durairajanayagam, Ashok Agarwal *, Chloe Ong Center for Reproductive Medicine, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio, USA * Corresponding author. E-mail address: [email protected] (A Agarwal). Damayanthi Durairajanayagam, PhD is a Senior Lecturer in Physiology at the Faculty of Medicine, MARA Univer- sity of Technology (UiTM), Malaysia. She is a past recipient of the Fulbright Research Exchange Scholar Award and recently completed her Research Fellowship at the Center for Reproductive Medicine, Cleveland Clinic, USA. Her research interests include oxidative stress, antioxidants and male infertility, and the use of proteomics and bioinformatics in studying the molecular markers of oxidative stress in infertile males. Abstract The process of spermatogenesis is temperature-dependent and occurs optimally at temperatures slightly lower than that of the body. Adequate thermoregulation is imperative to maintain testicular temperatures at levels lower than that of the body core. Raised testicular temperature has a detrimental effect on mammalian spermatogenesis and the resultant spermatozoa. Therefore, thermoregulatory failure leading to heat stress can compromise sperm quality and increase the risk of infertility. In this paper, several different types of external and internal factors that may contribute towards testicular heat stress are reviewed. The effects of heat stress on the process of spermatogenesis, the resultant epididymal spermatozoa and on germ cells, and the consequent changes in the testis are elaborated upon. We also discuss the molecular response of germ cells to heat exposure and the possible mechanisms involved in heat-induced germ cell damage, including apoptosis, DNA damage and autophagy. Further, the intrinsic and extrinsic pathways that are involved in the intricate mechanism of germ cell apoptosis are explained. Ultimately, these complex mechanisms of apoptosis lead to germ cell death. © 2014 Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved. KEYWORDS: germ cell apoptosis, male infertility, molecular mechanisms, risk factors, scrotal hyperthermia, sperm DNA damage Introduction (Zhu et al., 2004). Spermatozoa resulting from sperm cells exposed to hyperthermia in mice undergo apoptosis (Yin et al., 1997b) and contain damaged DNA (Perez-Crespo et al., 2008), The lack of thermoregulation of scrotal temperature causes leading to poor fertilizing capacity in vivo and in vitro (Yaeram testicular hyperthermia, which leads to genital heat stress. et al., 2006). This is detrimental to spermatogenesis and results in sper- Significant apoptotic loss of germ cells after testicular heat matozoa of inferior quality. Both the epididymal sperm and stress may occur either through intrinsic or extrinsic path- testicular germ cells are sensitive to damage by heat stress ways. The molecular events that arise in germ cells exposed http://dx.doi.org/10.1016/j.rbmo.2014.09.018 1472-6483/© 2014 Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved. Please cite this article in press as: Damayanthi Durairajanayagam, Ashok Agarwal, Chloe Ong, Causes, effects and molecular mechanisms of testicular heat stress, Repro- ductive BioMedicine Online (2014), doi: 10.1016/j.rbmo.2014.09.018 ARTICLE IN PRESS 2 D Durairajanayagam et al. to heat stress include the pro-apoptotic Bax and anti-apoptotic testis, followed by spermiogenesis in the epididymis. Human Bcl-2, cytochrome C, caspases and other heat-induced factors spermatogenesis requires almost 74 days for a complete cycle, (Kim et al., 2013). The germ cell apoptosis response that whereas sperm cells complete epididymal maturation in about follows heat stress takes place in a developmental stage- 12 days. The sequential cellular events of the spermato- specific manner, with the spermatocytes (diplotene and pachy- genic process initiate at the basal compartment and con- tene) and spermatids being most prone to heat-induced clude at the apical compartment of the seminiferous tubules. changes (Lue et al., 1999; Setchell, 1998). The reason for this Testosterone plays a crucial role in maintaining normal sper- vulnerability, however, has not been elucidated. matogenesis at the seminiferous tubules. The severity of damage to sperm cells subjected to heat stress varies with the intensity, frequency and duration of heat Events at the basal compartment of the exposure (Collins and Lacy, 1969; Paul et al., 2008). When seminiferous tubules germ cell apoptosis occurs it is also influenced by the sever- ity and duration of heat stress (Kim et al., 2013). The two main events that occur here are during spermato- In this review, the following are discussed: the effects of goniogenesis (type Apale spermatogonia renews itself to hyperthermia on spermatogenesis, the measurement methods generate the stem cell pool), and type Apale (spermato- of scrotal temperatures, the various modifiable and non- gonia develop into Type B spermatogonia), which pro- modifiable factors that could cause increased testicular tem- gress to preleptotene, followed by leptotene primary peratures, the molecular mechanism of apoptosis, DNA damage spermatocytes. and autophagy, changes in gene expression and the path- ways of germ cell apoptosis in response to testicular heat stress. Events at the apical compartment of the seminiferous tubules Effects of heat stress on spermatogenesis The three main events that occur here are spermatocy- and testis togenesis (primary spermatocytes progress from zygotene, pachytene, diplotene stages, to secondary spermatocytes then Testicular thermoregulation haploid spermatids); early round spermatids develop into elon- gated spermatids and undergo spermiogenesis to form sper- For optimal spermatogenesis to occur, testicular tempera- matozoa with fully compacted chromatin; and spermiation tures are maintained 2–4°C lower than core body tempera- (maturation and subsequent release of spermatozoa into semi- ture (Mieusset and Bujan, 1995). The temperature within the niferous lumen). testes is reflected by the temperature of the surrounding scrotal sac. Thermoregulation of the testis is aided by several Spermiation and maturation in the epididymis characteristics of the scrotal sac, such as thin skin with minimal subcutaneous fat, dense sweat glands and scant hair distri- Once in the lumen, spermatozoa leave the testis through bution. The musculature and vasculature in the genitals play rete testis into the epididymis, where sperm cells increase a role in regulating testicular temperature as well. To maxi- in concentration (caput), undergo maturation (corpus), and mize heat loss, the cremaster muscle that surrounds the testes are stored (cauda). Sperm cells at the tail end of the epi- and spermatic cords and the dartos muscle that lies beneath didymis have achieved full maturation, fertilizing ability and the scrotal skin relax, causing the testes to hang away from motility. the abdomen and the scrotal skin to slacken, increasing the total surface area for easy heat dissipation. Further, vaso- Naturally occurring defects during spermatogenesis dilation of scrotal vessels and activation of sweat glands The spermatogenic potential for human reproduction is a mere promote heat loss when temperatures increase. 12%, as the remaining sperm cells that develop either de- The testis is also thermoregulated via the counter-current generate, undergo apoptosis or develop abnormally (Sharpe, mechanism. Testicular artery and veins facilitate heat ex- 1994). Defects may occur during any part of spermatogenic change from the ‘warmer’ inflowing arterial blood to the cooler process. In spermatogoniogenesis, failure of Type A sper- outgoing venous blood. This transfer of heat assures that pale matogonia to develop into Type B spermatogonia leads to sper- ‘cooler’ arterial blood reaches the testis while the ‘warmed’ matogenic arrest (Holstein et al., 1988). During a defective venous blood disperses heat through the thin, scrotal skin ( Glad meiotic phase, apoptotic spermatocytes and spermatogenic Sorensen et al., 1991). Testicular veins carrying the ‘warm’ arrest of primary spermatocytes may occur. The cytoplasm blood anastomose and drain into the pampiniform plexus. In (cytoplasmic droplet) of the immature sperm cell is elimi- the case of varicocele, the pampiniform plexus becomes nated in spermiation, however, in some defective sperma- dilated, causing stasis and backflow of ‘warm’ blood back into tozoa, the cytoplasm may still remain as excess residual the internal spermatic veins. The compromised counter- cytoplasm (Breucker et al., 1985). During spermiogenesis, when current heat exchange thereby contributes to the increased haploid spermatids transform into fully differentiated sper- testicular temperatures found in varicocele patients ( Setchell, matozoa, defects that may occur (which are likely attribut- 1998). able to genetic factors) include absence of the acrosome, absence of the midpiece of the flagellum and damaged nuclear Spermatogenesis condensation (Holstein et al., 2003). Defects in the morphol- ogy of the ejaculated spermatozoa (head, neck, midpiece, The developmental process of the male gamete involves sper- tail, or all) are commonly seen during analysis of the seminal matogenesis in the lumen of the seminiferous tubules in the fluid (WHO, 2010).
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